ISSN: 1524-4563
Copyright © 1998 American Heart Association. All rights reserved. Print ISSN: 0194-911X. Online 72514
Hypertension is published by the American Heart Association. 7272 Greenville Avenue, Dallas, TX
1998;32;584-587 Hypertension
Carugo, Matteo Denti and Giuseppe Mancia
Cristina Giannattasio, Monica Failla, Alessandra Grappiolo, Marco Bigoni, Stefano Properties
Effects of Prolonged Immobilization of the Limb on Radial Artery Mechanical
http://hyper.ahajournals.org/cgi/content/full/32/3/584 located on the World Wide Web at:
The online version of this article, along with updated information and services, is
http://www.lww.com/reprints
Reprints: Information about reprints can be found online at
journalpermissions@lww.com 410-528-8550. E-mail:
Kluwer Health, 351 West Camden Street, Baltimore, MD 21202-2436. Phone: 410-528-4050. Fax:
Permissions: Permissions & Rights Desk, Lippincott Williams & Wilkins, a division of Wolters
http://hyper.ahajournals.org/subscriptions/
Subscriptions: Information about subscribing to Hypertension is online at
Artery Mechanical Properties
Cristina Giannattasio, Monica Failla, Alessandra Grappiolo, Marco Bigoni, Stefano Carugo, Matteo Denti, Giuseppe Mancia
Abstract—Physical training is associated with an increase in arterial distensibility. Whether the effect of training on this variable is evident also for ordinary levels of exercise or no exercise is unknown, however. We have addressed this issue by investigating the effect on radial artery distensibility of prolonged monolateral immobilization of the ipsilateral limb versus the following resumption of normal mobility. We studied 7 normotensive subjects (age, 25.4 63.0 years; systolic/diastolic blood pressure, 119 69/6866 mm Hg, mean6SE) in whom 1 limb had been immobilized for 30 days in plaster because of a fracture of the elbow. At both the day after plaster removal and after 45 days of rehabilitation, radial artery distensibility was evaluated by an echo-tracking device (NIUS-02), which allows arterial diameter to be measured noninvasively and continuously over all pressures from diastole to systole (finger monitoring), with the distensibility values being continuously derived from the Langewouters formula. In both instances, the contralateral arm was used as control. Immediately after removal of the plaster, radial artery distensibility was markedly less in the previously immobilized and fractured limb compared with the contralateral limb (0.4 60.1 versus 0.860.1, 1/mm Hg 10
23, P ,0.05). After rehabilitation, the distensibility of the radial artery was markedly increased in the previously fractured limb (0.65 60.1 1/mm Hg 10
23, P ,0.05), whereas no change was seen in the contralateral limb. Thus, complete interruption of physical activity is associated with a marked reduction of arterial distensibility, indicating that even an ordinary level of activity plays a major role in modulation of arterial mechanical properties. (Hypertension. 1998;32:584-587.)
Key Words: arterial distensibility n training n exercise n vessels n circulation
E xercise training is associated with several changes in car- diac and arteriolar structure and function.1–9 There is evi- dence, however, that large and conduit artery mechanical prop- erties are also modified by training and that the modification consists of an increase in distensibility
10 –13that is particularly evident in the arteries of the limbs most involved in the physical activity.
14
Whether arterial mechanical properties are modified also by ordinary levels of physical activity (rather than becoming manifest only during exercise training) has never been investigated. In the present study, we addressed this issue by measuring radial artery diameter and distensibility in subjects in whom 1 arm was immo- bilized in plaster for 30 days because of an elbow fracture. The examination was performed on the day after removal of the plaster and after 45 days of rehabilitation, in both instances using the contralateral radial artery as control.
Methods Subjects
We studied 7 healthy, right-handed young subjects (5 males, 2 females) aged from 17 to 30 years (25.463.0 years, mean6SE). The subjects suffered from elbow fracture that had been treated by complete immobilization of the limb in plaster for 30 days. All subjects had sphygmomanometric blood pressure values,140/90 mm Hg (mean of
3 measurements). They volunteered to participate in the study after being informed of its nature and purpose. The study protocol was approved by the ethics committee of our hospital.
Radial Artery Evaluation
In the present study, the time-dependent changes in arterial diameter were obtained with an A-mode ultrasonic echo-tracking device that recorded the displacement of the radial artery over the whole cardiac cycle (NIUS-02 system, Asulab, and Capital Medical Service)15 and thus over the whole diastolo-systolic pressure range. Briefly, the device uses a highly focalized transducer operating at a frequency of 10 MHz that was stereotaxically positioned over the radial artery 2 to 4 cm above the wrist, with gel used as a medium to prevent direct contact with the skin. With the subject supine and the arm immobile at the heart level, the transducer was oriented perpendicularly to the longitudinal axis and the largest cross-sectional dimension of the artery, based on the Doppler acoustic quality signal. After the switch to A-mode, the echo beams corresponding to the inner posterior and anterior walls of the artery were visualized on a computer screen (via an analog/digital fast transducer), thus allowing internal diameter variations to be derived. The spatial resolution was 150mm.15The internal diameter of the pulsating radial artery was measured at 50 Hz, and the device resolution allowed the identification of diameter changes of 0.0025 mm during the blood pressure cycle15,16(see below).
The device also uses a photoplethysmographic system (Finapres, Ohmeda) that allows blood pressure to be recorded noninvasively from a finger ipsilateral to the radial artery examined with an accuracy similar to intra-arterial radial artery pressure17and with a resolution of 2 mm Hg.17
Received February 2, 1998; first decision February 17, 1998; revision accepted April 8, 1998.
From the Cattedre di Medicina Interna (C.G., M.F., A.G., S.C., G.M.) and Ortopedia (M.B., M.D.), Universita` di Milano and Ospedale S. Gerardo, Monza; and the Centro di Fisiologia Clinica e Ipertensione, IRCSS Ospedale Maggiore, Milano (G.M.), Italy.
Correspondence to Professor Giuseppe Mancia, Clinica Medica, Universita` di Milano, Ospedale S. Gerardo dei Tintori, via Donizetti 106, 20052 Monza, Milano, Italy. E-mail mancia.g@imiucca.csi.unimi.it
© 1998 American Heart Association, Inc.
584
Blood pressure and arterial diameter signals were directed to a computer that was programmed to calculate the cross-sectional/pressure curve of the vessel. The curve was analyzed according to its fit with the arctangent model of Langewouters et al,18which is based on the formula
S5a
F
p21tan21S
P2bgDG
where S is the cross-sectional area of the vessel, P is the intravascular pressure, anda, b, and g are 3 optimal parameters describing the spatial position of the diameter-pressure curve.18From this formula, cross-sectional compliance (C5DS/DP19) was calculated as follows:
C5a g
1 11
S
P2bgD
2and expressed as consecutive values for blood pressure ranging from diastole to systole (cross-sectional compliance/pressure curve). The above formula was then used to calculate cross-sectional distensi- bility (cross-sectional compliance divided by vessel section) over the blood pressure range from diastole to systole (cross-sectional disten- sibility/pressure curve).
All measurements were performed by a single operator. The variation coefficient of radial artery diameter measurements obtained by the same operator in 2 different sessions (the within-operator variability) was 3.0%. The corresponding variation coefficient of radial artery cross-sectional distensibility was 7.0%.
Protocol and Data Analysis
The study was conducted on the morning of the day after removal of the plaster, following a 12-hour abstinence from alcohol consumption, caffeine consumption, and smoking. The protocol of the study was as follows: (1) Each subject was placed in the supine position and fitted with the finger pressure and the echo-tracking devices after exclusion of the presence of edema at the measurement sides. (2) After a 10-minute interval, radial artery diameter and cross-sectional distensibility were continuously measured over a 15-minute baseline period together with blood pressure and heart rate. The measurements were performed first in 1 limb and then in the contralateral limb, the first measuring side being
selected randomly. (3) The whole procedure was repeated following the same sequence after 45 days of rehabilitation of the healed limb.
Rehabilitation included intermittent handgrip exercise of the forearm muscles (squeezing a ball) and repeated flexion and extension of the forearm for 30 minutes per day.
Blood pressure, heart rate, and radial artery diameter and distensibil- ity were obtained by averaging the values of five 30-second periods taken at 3-minute intervals. Radial artery diameter/pressure curves, cross-sectional distensibility/pressure curves, and diameter at diastolic blood pressure obtained in individual subjects were summed and expressed as mean values for the group as a whole, separately for either arm and either experimental condition. This was done also for the area under the curve relating cross-sectional distensibility to blood pressure normalized for pulse pressure, ie, the “distensibility index.”20 –24
The statistical significance of the differences in mean values between arms and situations was assessed by 2-way ANOVA. The 2-tailed unpaired Student t test was used to locate differences between arms, whereas the paired Student t test was used to locate differences before and after rehabilitation. Throughout the text, values are mean6SEM.
Results
Figure 1, left panels, shows that in the study performed immediately after the removal of the plaster, the increase in blood pressure from diastole to systole was accompanied by a slight progressive increase in radial artery diameter and by a steep progressive and nonlinear reduction in radial artery distensibility; this was the case in both the previously immobilized limb and the contralateral limb. In the previ- ously immobilized limb, radial artery diameter was only slightly less than in the contralateral limb (Figure 1, right top). Radial artery distensibility, however, was much smaller, the difference in the distensibility index being statistically significant (Figure 1, right bottom). This was the case also when the distensibility index was calculated for the portion of the 2 curves that shared the same blood pressure range, ie, the
“isobaric” distensibility index.
20 –24Figure 1. Radial artery diameter/blood pressure curves, distensibility/blood pressure curves, diastolic diameter, and distensibility index in the healed (H) and contralateral (C) arms. Data are mean6SE.
Giannattasio et al September 1998 585
As shown in Figure 2, systolic blood pressure, diastolic blood pressure, and heart rate were not modified after 45 days of rehabilitation of the healed limb, which showed a slight and not significant increase in radial artery diameter. Radial artery distensibility, however, increased significantly, and the difference in the distensibility index from the value seen immediately after removal of the plaster was statistically significant, which was also the case for the isobaric disten- sibility index. The rehabilitation period did not modify radial artery diameter and distensibility in the contralateral limb, for which the distensibility index value remained slightly greater than that of the healed limb even after rehabilitation.
The forearm circumference in the healed limb was 24.0 62.1 cm before and 26.162.0 cm after rehabilitation (P ,0.05). The corresponding values in the contralateral limb were 26.5 61.8 and 26.361.9 cm.
Discussion
Several studies have shown that exercise training is accompanied by an increase in arterial distensibility.
10–14The present study, however, offers the first demonstration that the effect of exercise on arterial
mechanical properties is not limited to that obtained by an increase in the exercise level but is already evident and marked for an ordinary level of physical activity. That is, that when arterial distensibility is quantified in a limb first after prolonged immobili- zation and then after physical rehabilitation, its value is much greater in the latter compared with the former condition. Physical activity should thus be regarded as a mechanism involved in the determination of arterial mechanical function in all subjects, its role coexisting with other mechanisms involved in the tonic modulation of these functions, eg, sympathetic nerve activity.
4,21,23,25–27Our study does not clarify the mechanisms responsible for the effect of an ordinary level of physical activity on arterial distensibility. We can speculate, however, that both structural and functional factors are involved. Structural factors may reflect the fact that immobilization may lead to a reduction of the more distensible components of the wall tissues (eg, smooth muscle and elastin) to a greater extent than a reduction in the stiffer components (eg, collagen).
28,29Functional factors may reflect the fact that immobilization leads to a local increase in sympathetic tone, given the evidence that sympathetic tone reduces radial artery distensibility, probably via contraction of smooth muscle in the arterial wall.
3,4,20,21,25They may also reflect the
Figure 2. Blood pressure, heart rate, distensi- bility/blood pressure curves, individual and mean distensibility indexes, and individual and mean diastolic diameters in the healed (H) and contralateral (C) limbs before (B) and after (A) mobilization. Data are mean6SE. S indi- cates systolic; D, diastolic. *P,0.01 vs con- trol; §P,0.05 vs before rehabilitation.fact that immobilization may be accompanied by a reduction in limb blood flow (as indirectly suggested by the reduced forearm circum- ference after immobilization) and thus in the shear stress–deter- mined endothelial secretion of substances (eg, nitric oxide) that relax vascular smooth muscle and make it more distensible than in the contracted state.
30–33Unfortunately, the structural hypothesis cannot be tested because of the need for a bioptic and thus invasive approach. The functional hypothesis, on the other hand, can be tested by examining whether a difference in arterial distensibility disappears in the period immediately after prolonged ischemia (ie, when smooth muscle tone in the arterial wall is completely abolished).
20,22,34This was not possible in our subjects, however, because of the difficulty of performing these maneuvers immedi- ately after removal of the plaster when effective skeletal muscle contraction and limb extension were impaired.
Our findings that an ordinary level of physical activity already exerts a positive influence on arterial distensibility has pathophysiological implications. We can speculate that sedentariness should be regarded as an unfavorable condition as far as large artery function is concerned, given the adverse consequences (increased cardiac work, greater reflection of pulse waves, greater central blood pressure, greater trauma to the vessel wall) that increased artery stiffness has on the cardiovascular system.
35We can also speculate that these consequences may develop in cardiovascular diseases, which are accompanied and characterized by a reduced level of physical activity, although the neurohumoral situation is different and complex; one of these could be congestive heart failure, in which radial artery distensibility has indeed been shown to be reduced.
21,23,26,36References
1. Coats AJ, Adamopoulos S, Radaelli A, McCance A, Meyer TE, Bernardi L, Solda PL, Davey P, Ormerod O, Forfar C. Controlled trial of physical training in chronic heart failure: exercise performance, hemodynamics, ventilation and autonomic function. Circulation. 1992;85:2119 –2131.
2. Sherer J, Tipton CN. Cardiovascular adaptation to physical training. Ann Rev Physiol. 1977;39:221–251.
3. Grassi G, Seravalle G, Calhoun DA, Mancia G. Physical training and baroreceptor control of sympathetic nerve activity in humans. Hyper- tension. 1994;23:294 –301.
4. Somers VK, Leo KC, Shields R, Clary M, Mark AL. Forearm endurance training attenuates sympathetic nerve response to isometric handgrip in normal humans. J Appl Physiol. 1992;72:1039 –1043.
5. Sinoway LI, Stenberger J, Wilson J, McLaughlin S, Musk T, Zelis R. A 30-day forearm work protocol increases maximal forearm blood flow.
J Appl Physiol. 1987;62:1063–1067.
6. Sinoway LI, Musch TI, Minotti J, Zelis R. Enhanced maximal metabolic vasodilatation in the dominant arm of tennis players. J Appl Physiol.
1986;61:673– 678.
7. Yang HT, Ogilvie RW, Terjung RL. Training increases collateral- dependent muscle blood flow in aged rats. Am J Physiol. 1995;268(3 pt 2):H1174 –H1180.
8. Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol. 1985;59:320 –327.
9. Klausen K, Andersen LB, Pelle I. Adaptative changes in work capacity, skeletal muscle capillarization and enzyme levels, during training and detraining. Acta Physiol Scand. 1981;113:9 –16.
10. Cameron JD, Dart AM. Exercise training increases total systemic arterial compliance in humans. Am J Physiol. 1994;266:H693–H701.
11. Kingwell BA, Cameron KJ, Gillies GL, Jennings GL, Dart AM. Arterial compliance may influence baroreflex function in athletes and hyper- tensives. Am J Physiol. 1995;268:H411–H418.
12. Mohiaddin RH, Underwood SR, Bogren HG, Firman DN, Klipstein RH, Rees RSO, Longmore DB. Regional aortic compliance studied by
magnetic resonance imaging: the effects of age, training and coronary artery disease. Br Heart J. 1989;62:90 –96.
13. Wijnen J, Kuipers H, Kool MJF, Hoeks APG, Van Baak MA, Struyker Boudier HAJ, Verstappen FTJ, Van Bortel LMAB. Vessel wall properties of large arteries in trained and sedentary subjects. Basic Res Cardiol.
1991;86(suppl 1):25–29.
14. Giannattasio C, Cattaneo B, Mangoni AA, Carugo S, Sampieri L, Cuspidi C, Grassi G, Mancia M. Changes in arterial compliance induced by physical training in hammer-throwers. J Hypertens. 1992;10(suppl 6):S53–S55.
15. Tardy Y, Meister JJ, Perret F, Brunner HR, Arditi M. Noninvasive estimate of the mechanical properties of peripheral arteries from ultrasonic and photoplethysmographic measurements. Clin Phys Physiol Meas. 1991;3:360 –367.
16. Girerd X, Mourad JJ, Acar C, Heudes B, Chiche S, Bruneval P, Mignot JP, Billaud E, Safar M, Laurent S. Noninvasive measurement of medium size artery wall thickness in humans: in vitro validation. J Vasc Res. 1994;31:114–120.
17. Parati G, Casadei A, Groppelli A, Di Rienzo M, Mancia G. Comparison of finger and intra-arterial blood pressure monitoring at rest and during laboratory testing. Hypertension. 1989;13:645– 647.
18. Langewouters GJ, Zwart A, Busse R, Wesseling KH. Pressure diameter relationship of segments of human finger arteries. Clin Phys Physiol Meas. 1986;7:43– 45.
19. Dobrin PB. Vascular mechanics. In: Shepherd JT, Abboud FM, eds.
Handbook of Physiology, Section 2: The Cardiovascular System. Vol III, Part I: Peripheral Circulation and Organ Blood Flow. Bethesda, Md:
American Physiological Society; 1983:65–102.
20. Giannattasio C, Mangoni AA, Stella ML, Carugo S, Grassi G, Mancia G.
Acute effects of smoking on radial artery compliance in humans.
J Hypertens. 1994;12:691– 696.
21. Giannattasio C, Failla M, Stella ML, Mangoni AA, Carugo S, Pozzi M, Grassi G, Mancia G. Alterations of radial artery compliance in patients with congestive heart failure. Am J Cardiol. 1995;76:381–385.
22. Giannattasio C, Mangoni AA, Failla M, Carugo S, Stella ML, Stefanoni P, Grassi G, Vergani C, Mancia G. Impaired radial artery compliance in normotensive subjects with familial hypercholesterolemia. Atherosclero- sis. 1996;124:249 –260.
23. Giannattasio C, Failla M, Stella ML, Mangoni AA, Turrini D, Carugo S, Pozzi M, Grassi G, Mancia G. Angiotensin-converting enzyme inhibition and radial artery compliance in patients with congestive heart failure.
Hypertension. 1995;26:491– 496.
24. Laurent S, Girerd X, Mourad JJ, Lacolley P, Beck L, Boutouyrie P, Mignot JP, Safar M. Elastic modulus of the radial artery wall material is not increased in patients with essential hypertension. Arterioscler Thromb. 1994;14:1223–1231.
25. Grassi G, Giannattasio C, Failla M, Pesenti A, Peretti G, Marinoni E, Fraschini N, Vailati S, Mancia G. Sympathetic modulation of radial artery compliance in congestive heart failure. Hypertension. 1995;26:348 –354.
26. Hayoz D, Weber WR, Rutschmann B, Darioli R, Burnier M, Waeber B, Brunner H. Postischemic blood flow response in hypercholesterolemic patients. Hypertension. 1995;26:497–502.
27. Mangoni AA, Mircoli L, Giannattasio C, Ferrari AU, Mancia G. Heart rate- dependence of arterial distensibility in vivo. J Hypertens. 1996;14:897–901.
28. Clark JM, Glagov S. Transmural organization of the arterial media the lamellar unit revisited. Atherosclerosis. 1985;5:19 –34.
29. Glagov S, Vito R, Giddens DP, Zarins CK. Micro-architecture and com- position of artery walls: relationship to location, diameter and the distri- bution of mechanical stress. J Hypertens. 1992;10(suppl 6):S101–S104.
30. Rubanyi GM, Romero JC, Vanhoutte PM. Flow-induced release of endothe- lium-derived relaxing factor. Am J Physiol. 1988;250:H1145–H1149.
31. Clausen JP, Klausen K, Rasmussen B, Trap-Jensen J. Central and periph- eral circulatory changes after training of the arms or legs. Am J Physiol.
1973;225:675– 682.
32. Hutcheson IR, Griffith TM. Release of endothelium-derived relaxing factor is modulated by both frequency and amplitude of pulsatile flow.
Am J Physiol. 1991;261:H257–H262.
33. Delp MD, McAllister RM, Laughlin MH. Exercise training alters endo- thelium-dependent vasoreactivity of rat abdominal aorta. J Appl Physiol.
1993;75:1354 –1363.
34. Folkow B, Gribby G, Thulesius O. Adaptative structural changes of the vascular walls in hypertension and their relation to the control of the peripheral resistance. Acta Physiol Scand. 1958;44:255–272.
35. Nichols WWP, O’Rourke MF. McDonald’s Blood Flow in Arteries. 3rd ed. London, UK: E Arnold; 1990.
36. Burkhard H, Volker M, Drexler H. Physical training improves endothelial function in patients with chronic heart failure. Circulation. 1996;93:210 –214.
